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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Rampant Gene Loss in the Underground Orchid <italic>Rhizanthella gardneri</italic> Highlights Evolutionary Constraints on Plastid Genomes</title><author><name sortKey="Delannoy, Etienne" sort="Delannoy, Etienne" uniqKey="Delannoy E" first="Etienne" last="Delannoy">Etienne Delannoy</name><affiliation><nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Perth, Australia</nlm:aff></affiliation><affiliation><nlm:aff id="aff2">Laboratoire de Biologie du Développement des Plantes, Commissariat à l'Energie Atomique, Cadarache, St. Paul Les Durances, France</nlm:aff></affiliation></author><author><name sortKey="Fujii, Sota" sort="Fujii, Sota" uniqKey="Fujii S" first="Sota" last="Fujii">Sota Fujii</name><affiliation><nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Perth, Australia</nlm:aff></affiliation></author><author><name sortKey="Colas Des Francs Small, Catherine" sort="Colas Des Francs Small, Catherine" uniqKey="Colas Des Francs Small C" first="Catherine" last="Colas Des Francs-Small">Catherine Colas Des Francs-Small</name><affiliation><nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Perth, Australia</nlm:aff></affiliation></author><author><name sortKey="Brundrett, Mark" sort="Brundrett, Mark" uniqKey="Brundrett M" first="Mark" last="Brundrett">Mark Brundrett</name><affiliation><nlm:aff id="aff3">School of Plant Biology, University of Western Australia, Perth, Australia</nlm:aff></affiliation></author><author><name sortKey="Small, Ian" sort="Small, Ian" uniqKey="Small I" first="Ian" last="Small">Ian Small</name><affiliation><nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Perth, Australia</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">21289370</idno><idno type="pmc">3112369</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3112369</idno><idno type="RBID">PMC:3112369</idno><idno type="doi">10.1093/molbev/msr028</idno><date when="2011">2011</date><idno type="wicri:Area/Pmc/Corpus">002763</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002763</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Rampant Gene Loss in the Underground Orchid <italic>Rhizanthella gardneri</italic> Highlights Evolutionary Constraints on Plastid Genomes</title><author><name sortKey="Delannoy, Etienne" sort="Delannoy, Etienne" uniqKey="Delannoy E" first="Etienne" last="Delannoy">Etienne Delannoy</name><affiliation><nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Perth, Australia</nlm:aff></affiliation><affiliation><nlm:aff id="aff2">Laboratoire de Biologie du Développement des Plantes, Commissariat à l'Energie Atomique, Cadarache, St. Paul Les Durances, France</nlm:aff></affiliation></author><author><name sortKey="Fujii, Sota" sort="Fujii, Sota" uniqKey="Fujii S" first="Sota" last="Fujii">Sota Fujii</name><affiliation><nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Perth, Australia</nlm:aff></affiliation></author><author><name sortKey="Colas Des Francs Small, Catherine" sort="Colas Des Francs Small, Catherine" uniqKey="Colas Des Francs Small C" first="Catherine" last="Colas Des Francs-Small">Catherine Colas Des Francs-Small</name><affiliation><nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Perth, Australia</nlm:aff></affiliation></author><author><name sortKey="Brundrett, Mark" sort="Brundrett, Mark" uniqKey="Brundrett M" first="Mark" last="Brundrett">Mark Brundrett</name><affiliation><nlm:aff id="aff3">School of Plant Biology, University of Western Australia, Perth, Australia</nlm:aff></affiliation></author><author><name sortKey="Small, Ian" sort="Small, Ian" uniqKey="Small I" first="Ian" last="Small">Ian Small</name><affiliation><nlm:aff id="aff1">Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Perth, Australia</nlm:aff></affiliation></author></analytic><series><title level="j">Molecular Biology and Evolution</title><idno type="ISSN">0737-4038</idno><idno type="eISSN">1537-1719</idno><imprint><date when="2011">2011</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Since the endosymbiotic origin of chloroplasts from cyanobacteria 2 billion years ago, the evolution of plastids has been characterized by massive loss of genes. Most plants and algae depend on photosynthesis for energy and have retained ∼110 genes in their chloroplast genome that encode components of the gene expression machinery and subunits of the photosystems. However, nonphotosynthetic parasitic plants have retained a reduced plastid genome, showing that plastids have other essential functions besides photosynthesis. We sequenced the complete plastid genome of the underground orchid, <italic>Rhizanthella gardneri</italic>. This remarkable parasitic subterranean orchid possesses the smallest organelle genome yet described in land plants. With only 20 proteins, 4 rRNAs, and 9 tRNAs encoded in 59,190 bp, it is the least gene-rich plastid genome known to date apart from the fragmented plastid genome of some dinoflagellates. Despite numerous differences, striking similarities with plastid genomes from unrelated parasitic plants identify a minimal set of protein-encoding and tRNA genes required to reside in plant plastids. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Mol Biol Evol</journal-id><journal-id journal-id-type="hwp">molbiolevol</journal-id><journal-id journal-id-type="publisher-id">molbev</journal-id><journal-title-group><journal-title>Molecular Biology and Evolution</journal-title></journal-title-group><issn pub-type="ppub">0737-4038</issn><issn pub-type="epub">1537-1719</issn><publisher><publisher-name>Oxford University Press</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">21289370</article-id><article-id pub-id-type="pmc">3112369</article-id><article-id pub-id-type="doi">10.1093/molbev/msr028</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Articles</subject></subj-group></article-categories><title-group><article-title>Rampant Gene Loss in the Underground Orchid <italic>Rhizanthella gardneri</italic> Highlights Evolutionary Constraints on Plastid Genomes</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Delannoy</surname><given-names>Etienne</given-names></name><xref ref-type="corresp" rid="cor1">*</xref><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Fujii</surname><given-names>Sota</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Colas des Francs-Small</surname><given-names>Catherine</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Brundrett</surname><given-names>Mark</given-names></name><xref ref-type="aff" rid="aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Small</surname><given-names>Ian</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib></contrib-group><aff id="aff1"><label>1</label>Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Perth, Australia</aff><aff id="aff2"><label>2</label>Laboratoire de Biologie du Développement des Plantes, Commissariat à l'Energie Atomique, Cadarache, St. Paul Les Durances, France</aff><aff id="aff3"><label>3</label>School of Plant Biology, University of Western Australia, Perth, Australia</aff><author-notes><corresp id="cor1"><label>*</label><bold>Corresponding author:</bold> E-mail: <email>delannoy@evry.inra.fr</email>.</corresp><fn><p><bold>Associate editor</bold>: Charles Delwiche</p></fn></author-notes><pub-date pub-type="ppub"><month>7</month><year>2011</year></pub-date><pub-date pub-type="epub"><day>2</day><month>2</month><year>2011</year></pub-date><pub-date pub-type="pmc-release"><day>2</day><month>2</month><year>2011</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>28</volume><issue>7</issue><fpage>2077</fpage><lpage>2086</lpage><permissions><copyright-statement>© The Author(s) 2011. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.</copyright-statement><copyright-year>2011</copyright-year><license license-type="open-access"><license-p><pmc-comment>CREATIVE COMMONS</pmc-comment>This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc/2.5">http://creativecommons.org/licenses/by-nc/2.5</ext-link>), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p></license></permissions><abstract><p>Since the endosymbiotic origin of chloroplasts from cyanobacteria 2 billion years ago, the evolution of plastids has been characterized by massive loss of genes. Most plants and algae depend on photosynthesis for energy and have retained ∼110 genes in their chloroplast genome that encode components of the gene expression machinery and subunits of the photosystems. However, nonphotosynthetic parasitic plants have retained a reduced plastid genome, showing that plastids have other essential functions besides photosynthesis. We sequenced the complete plastid genome of the underground orchid, <italic>Rhizanthella gardneri</italic>. This remarkable parasitic subterranean orchid possesses the smallest organelle genome yet described in land plants. With only 20 proteins, 4 rRNAs, and 9 tRNAs encoded in 59,190 bp, it is the least gene-rich plastid genome known to date apart from the fragmented plastid genome of some dinoflagellates. Despite numerous differences, striking similarities with plastid genomes from unrelated parasitic plants identify a minimal set of protein-encoding and tRNA genes required to reside in plant plastids. This prime example of convergent evolution implies shared selective constraints on gene loss or transfer.</p></abstract><kwd-group><kwd><italic>Rhizanthella gardneri</italic></kwd><kwd>mycoheterotroph</kwd><kwd>chloroplast</kwd><kwd>tRNA import</kwd><kwd>gene loss</kwd></kwd-group></article-meta></front><body><sec sec-type="intro"><title>Introduction</title><p>Plastid-based photosynthesis is the primary energy source for life on Earth providing oxygen and sugars as the basis of almost every “food chain” scaling up from photosynthetic cells to whole ecosystems. Because the endosymbiosis of cyanobacteria by a nonphotosynthetic eukaryote cell, the evolution of plastids have been characterized by massive gene loss and transfer of most of the remainder to the nucleus (<xref ref-type="bibr" rid="bib45">Martin et al. 1998</xref>; <xref ref-type="bibr" rid="bib3">Archibald 2009</xref>). However, nonphotosynthetic plants, algae, and apicomplexan parasites such as <italic>Plasmodium</italic> sp. and <italic>Toxoplasma</italic> sp. have retained a plastid and a plastid genome or “plastome” (<xref ref-type="bibr" rid="bib66">Wolfe et al. 1992</xref>; <xref ref-type="bibr" rid="bib64">Wilson et al. 1996</xref>; <xref ref-type="bibr" rid="bib25">Funk et al. 2007</xref>) suggesting that the loss or transfer of DNA to the nucleus is limited by one or more essential nonphotosynthetic functions of plastids. Analyzing these functions in photosynthetic organisms is complex because perturbations of plastid metabolism have pleiotropic effects and are often deleterious or lethal (<xref ref-type="bibr" rid="bib1">Ahlert et al. 2003</xref>; <xref ref-type="bibr" rid="bib19">de Longevialle et al. 2008</xref>). The comparison of the plastid genomes from nonphotosynthetic plants should highlight these essential functions as well as the constraints preventing the transfer of genes from the plastid to the nucleus.</p><p>There are two distinctly different functional categories of plants that have partly or fully lost the capacity for photosynthesis: 1) parasites that exploit other plants via direct connections and 2) myco-heterotrophs that indirectly exploit other plants via mycorrhizal fungi (<xref ref-type="bibr" rid="bib11">Brundrett 2009</xref>). Both categories are referred to as parasites here. In total, there are about 13 evolutionary lineages of parasitic plants and at least 30 of myco-heterotrophs, almost all the latter within the orchid family (<xref ref-type="bibr" rid="bib11">Brundrett 2009</xref>; <xref ref-type="bibr" rid="bib62">Westwood et al. 2010</xref>). To date, the analysis of complete plastomes from parasitic plants has been restricted to dicots which are direct parasites of either roots (<italic>Orobanchaceae</italic>; <xref ref-type="bibr" rid="bib20">dePamphilis and Palmer 1990</xref>) or shoots (<italic>Cuscuta</italic>; <xref ref-type="bibr" rid="bib25">Funk et al. 2007</xref>) of other plants. No similar analysis has been published on the plastid genomes from nonphotosynthetic orchids that have a distinct evolutionary origin (the last common ancestor of orchids and dicots lived at least 120 Ma; <xref ref-type="bibr" rid="bib49">Ramirez et al. 2007</xref>), with a very different growth habit and a different mode of parasitism.</p><p>For this study, we chose the Western Underground Orchid (<italic>Rhizanthella gardneri</italic>; <xref ref-type="fig" rid="fig1">fig. 1<italic>A</italic></xref> and <italic><xref ref-type="fig" rid="fig1">B</xref></italic>) an iconic West Australian species. Remarkably, and unlike land plants from any other genus, the entire life cycle of <italic>R. gardneri</italic> occurs underground, with the flowers opening several centimeters below the soil surface. Its subterranean lifestyle ensures that it is incapable of photosynthesis; instead, it gains its energy and nutrients as a myco-heterotroph via <italic>Ceratobasidium</italic> fungi that form ectomycorrhizas with roots of broom bush, <italic>Melaleuca uncinata</italic> (<xref ref-type="fig" rid="fig1">fig. 1<italic>C</italic></xref>; <xref ref-type="bibr" rid="bib10">Bougoure et al. 2009</xref>, <xref ref-type="bibr" rid="bib9">2010</xref>). <italic>R. gardneri</italic> is critically endangered and known from only five locations in Western Australia (<xref ref-type="fig" rid="fig1">fig. 1<italic>D</italic></xref>), but related (and even rarer) species have been collected in Queensland and New South Wales, thousands of kilometers to the east, suggesting that these are ancient relictual species from a time before the center of Australia became arid, a process that started ∼15 Ma (<xref ref-type="bibr" rid="bib12">Byrne et al. 2008</xref>). Here, we report the full plastome sequence of <italic>R. gardneri</italic>. It is the smallest and most derived plastome described in land plants but shows strong evolutionary convergences with plastomes of other unrelated parasitic organisms.</p><fig id="fig1" position="float"><label>F<sc>IG</sc>. 1.</label><caption><p>Description of <italic>Rhizanthella gardneri</italic>. (<italic>A</italic>) Uncovered capitulum of <italic>R. gardneri</italic>. Picture courtesy of Susumu Yamaguchi. (<italic>B</italic>) Each capitulum encloses up to ∼50 flowers. (<italic>C</italic>) Typical habitat of <italic>R. gardneri</italic>, showing the host plant, <italic>Melaleuca uncinata</italic>. (<italic>D</italic>) Approximate known sites for <italic>R. gardneri</italic> in south-western Australia. Map from Google Earth.</p></caption><graphic xlink:href="molbiolevolmsr028f01_4c"></graphic></fig></sec><sec sec-type="materials|methods"><title>Materials and Methods</title><p>DNA was extracted from a capitulum of <italic>R. gardneri</italic> collected in the Munglinup area on the south coast of Western Australia. Due to the status of this endangered species, precise locations cannot be published. It was purified as described (<xref ref-type="bibr" rid="bib40">Lang and Burger 2007</xref>) except that plastid DNA could not be isolated from nuclear DNA by ultracentrifugation. Shotgun sequencing of total DNA was carried out on a Roche FLX system using the titanium kit (Roche Diagnostics, Castle Hill, NSW, Australia) at the Lotterywest State Biomedical Facility (Perth, WA, Australia). De novo assembly was performed with wgs (<xref ref-type="bibr" rid="bib47">Miller et al. 2008</xref>), which yielded four large plastid DNA contigs. After alignment on the <italic>Phalaenopsis aphrodite</italic> subsp. <italic>formosana</italic> plastid genome (AY916449) and manual editing of the assembly using the Seqman module of Lasergene 8 (DNASTAR, Madison, WI), the assembly of the contigs, gaps, and low coverage areas were verified by polymerase chain reaction (PCR) using primer pairs described in <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 1</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online, and PrimeSTAR DNA polymerase (Takara, Japan). tRNA detection was performed with Aragorn (<xref ref-type="bibr" rid="bib41">Laslett and Canback 2004</xref>) and by systematic alignment of <italic>P. aphrodite</italic> subsp. <italic>formosona</italic> plastid tRNA exons.</p><p>Total RNA from an aliquot of the sample used for DNA extraction was purified with acid phenol bromochloropropane (1/1) and precipitated with ethanol. RNAs were precipitated with LiCl before treatment with DNAfree DNAse (Ambion, Austin, TX). One microgram of total RNA was reverse transcribed with random primers and Superscript III (Invitrogen, Mount Waverley, VIC, Australia). <italic>rpl2</italic>, <italic>rpl16</italic>, and <italic>clpP</italic> cDNAs were amplified with the primers pairs described in <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 1</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online, and PrimeSTAR DNA polymerase (Takara, Japan).</p><p>To assess the variability of the plastid genome, DNA was extracted from a bract of <italic>R. gardneri</italic> collected in the Corrigin area (WA, Australia) and purified as described above. Fragments covering 32.9% of the plastid genome (accession numbers GU066242–GU066252) were sequenced using the primers pairs described in <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 1</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online, and the PrimeSTAR DNA polymerase (Takara, Japan). <italic>R. gardneri</italic> mitochondrial sequences among the library of reads from the FLX system were identified by similarity to rice mitochondrial DNA. For each open reading frame (ORF), the matching reads were assembled with Seqman (Lasergene 8, DNASTAR, Madison, WI). Because of low coverage, only partial sequences could be recovered for most coding sequences (CDS) except <italic>atp4</italic>, <italic>cox3</italic>, and <italic>nad9</italic> genes. The corresponding sequences from samples collected in the Munglinup area (accession numbers GU066236, GU066239, and GU066241) and the Corrigin area (accession numbers GU066237, GU066238, and GU066240) were produced as described above using primer pairs described in <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 1</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online. Sequence alignments were performed using MUSCLE (<xref ref-type="bibr" rid="bib24">Edgar 2004</xref>) and manually edited. The gene lists of 172 complete plastid genomes were collected from National Center for Biotechnology Information and manually curated (<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 2</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online). Duplicates within each genome were discarded as well as hypothetical ORFs without homologs. Using this matrix, the genomes were clustered by Bayesian inference using MrBayes 3.1 (<xref ref-type="bibr" rid="bib52">Ronquist and Huelsenbeck 2003</xref>).</p></sec><sec sec-type="results"><title>Results</title><p>Given the rarity of <italic>R. gardneri</italic>, biological material is extremely limited and insufficient for isolation of plastids. We estimated the proportion of plastid DNA in a total <italic>R. gardneri</italic> DNA preparation by quantitative PCR and calculated that it should be possible to achieve sufficient coverage of the plastid genome from a single sequencing run on total DNA. This prediction turned out to be well founded, and we assembled the 59,190 bp genome sequence (GenBank accession GQ413967) with an average of 15.7-fold coverage by shotgun deep sequencing of total DNA and targeted PCR amplifications to fill three short gaps and verify homopolymer runs.</p><p>The <italic>R. gardneri</italic> plastome (<xref ref-type="fig" rid="fig2">fig. 2</xref>) contains two inverted repeats (IR) of 9,767 bp, a large single-copy region of 26,361 bp, and a small single-copy region of 13,295 bp. This is the smallest known land plant organelle genome, being smaller than the plastid genome of the nonphotosynthetic dicot parasite <italic>Epifagus virginiana</italic> (<xref ref-type="bibr" rid="bib66">Wolfe et al. 1992</xref>). The synteny with the plastome of the photosynthetic orchid <italic>P. aphrodite</italic> (<xref ref-type="bibr" rid="bib14">Chang et al. 2006</xref>) is perfect (<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary fig. 1</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online) despite rampant gene loss. Unlike any other plastome with large IRs (<xref ref-type="bibr" rid="bib57">Strauss et al. 1988</xref>; <xref ref-type="bibr" rid="bib13">Cai et al. 2008</xref>), the ribosomal RNA (rRNA) genes are not included within them (<xref ref-type="fig" rid="fig2">fig. 2</xref>). The <italic>R. gardneri</italic> plastome has a high proportion of noncoding DNA (<xref ref-type="table" rid="tbl1">table 1</xref>). This is not primarily due to the presence of pseudogenes as there are only two obvious pseudogenes (<italic>rpl33</italic> and <italic>trnL</italic>) and two gene fragments (<italic>psaB</italic> and <italic>ndhK</italic>) covering 1.9% of the genome. Although easily detected by sequence alignments, the three <italic>rps12</italic> exons predict an RPS12 protein lacking some highly conserved amino acids at the C-terminus and we failed to detect any transspliced <italic>rps12</italic> mRNA, leading us to consider <italic>rps12</italic> as a third pseudogene.</p><table-wrap id="tbl1" position="float"><label>Table 1.</label><caption><p>Global Features of Selected Plastomes.</p></caption><table frame="hsides" rules="groups"><thead><tr><td rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1">Size (kb)</td><td align="center" rowspan="1" colspan="1">% Noncoding DNA<xref ref-type="table-fn" rid="tblfn1">a</xref></td><td align="center" rowspan="1" colspan="1">Coding Capacity<xref ref-type="table-fn" rid="tblfn2">b</xref></td><td align="center" rowspan="1" colspan="1">Number of Pseudogenes</td><td align="center" rowspan="1" colspan="1">Number of tRNAs<xref ref-type="table-fn" rid="tblfn3">c</xref></td><td align="center" rowspan="1" colspan="1">Accession Number</td></tr></thead><tbody><tr><td colspan="7" rowspan="1">Angiosperms</td></tr><tr><td rowspan="1" colspan="1"> <italic>Rhizanthella gardneri</italic></td><td align="char" char="." rowspan="1" colspan="1">59.2</td><td align="char" char="." rowspan="1" colspan="1">45.1</td><td align="char" char="." rowspan="1" colspan="1">33</td><td align="char" char="." rowspan="1" colspan="1">5</td><td align="char" char="." rowspan="1" colspan="1">9</td><td rowspan="1" colspan="1">GQ413967</td></tr><tr><td rowspan="1" colspan="1"> <italic>Phalaenopsis aphrodite</italic></td><td align="char" char="." rowspan="1" colspan="1">149</td><td align="char" char="." rowspan="1" colspan="1">49.8</td><td align="char" char="." rowspan="1" colspan="1">95</td><td align="char" char="." rowspan="1" colspan="1">7</td><td align="char" char="." rowspan="1" colspan="1">27</td><td rowspan="1" colspan="1">NC_007499</td></tr><tr><td rowspan="1" colspan="1"> <italic>Epifagus virginiana</italic></td><td align="char" char="." rowspan="1" colspan="1">70</td><td align="char" char="." rowspan="1" colspan="1">41.2</td><td align="char" char="." rowspan="1" colspan="1">40</td><td align="char" char="." rowspan="1" colspan="1">18</td><td align="char" char="." rowspan="1" colspan="1">15</td><td rowspan="1" colspan="1">NC_001568</td></tr><tr><td rowspan="1" colspan="1"> <italic>Cuscuta obtusiflora</italic></td><td align="char" char="." rowspan="1" colspan="1">85.3</td><td align="char" char="." rowspan="1" colspan="1">29.2</td><td align="char" char="." rowspan="1" colspan="1">85</td><td align="char" char="." rowspan="1" colspan="1">1</td><td align="char" char="." rowspan="1" colspan="1">23</td><td rowspan="1" colspan="1">NC_009949</td></tr><tr><td rowspan="1" colspan="1"> <italic>C. exaltata</italic></td><td align="char" char="." rowspan="1" colspan="1">125.4</td><td align="char" char="." rowspan="1" colspan="1">44.8</td><td align="char" char="." rowspan="1" colspan="1">96</td><td align="char" char="." rowspan="1" colspan="1">7</td><td align="char" char="." rowspan="1" colspan="1">27</td><td rowspan="1" colspan="1">NC_009963</td></tr><tr><td rowspan="1" colspan="1"> <italic>Nicotiana tabacum</italic></td><td align="char" char="." rowspan="1" colspan="1">155.9</td><td align="char" char="." rowspan="1" colspan="1">53.5</td><td align="char" char="." rowspan="1" colspan="1">110</td><td align="char" char="." rowspan="1" colspan="1">1</td><td align="char" char="." rowspan="1" colspan="1">28</td><td rowspan="1" colspan="1">NC_001879</td></tr><tr><td colspan="7" rowspan="1">Chlorophyta</td></tr><tr><td rowspan="1" colspan="1"> <italic>Helicosporidium</italic> sp.</td><td align="char" char="." rowspan="1" colspan="1">37.5</td><td align="char" char="." rowspan="1" colspan="1">5.1</td><td align="char" char="." rowspan="1" colspan="1">53</td><td align="char" char="." rowspan="1" colspan="1">0</td><td align="char" char="." rowspan="1" colspan="1">24</td><td rowspan="1" colspan="1">NC_008100</td></tr><tr><td rowspan="1" colspan="1"> <italic>Euglena longa</italic></td><td align="char" char="." rowspan="1" colspan="1">73.3</td><td align="char" char="." rowspan="1" colspan="1">47.7</td><td align="char" char="." rowspan="1" colspan="1">56</td><td align="char" char="." rowspan="1" colspan="1">1</td><td align="char" char="." rowspan="1" colspan="1">26</td><td rowspan="1" colspan="1">NC_002652</td></tr><tr><td rowspan="1" colspan="1"> <italic>E. gracilis</italic></td><td align="char" char="." rowspan="1" colspan="1">143.2</td><td align="char" char="." rowspan="1" colspan="1">57.4</td><td align="char" char="." rowspan="1" colspan="1">86</td><td align="char" char="." rowspan="1" colspan="1">7</td><td align="char" char="." rowspan="1" colspan="1">26</td><td rowspan="1" colspan="1">NC_001603</td></tr><tr><td colspan="7" rowspan="1">Containing secondarily acquired red algal plastids</td></tr><tr><td rowspan="1" colspan="1"> <italic>Eimeria tenella</italic></td><td align="char" char="." rowspan="1" colspan="1">34.8</td><td align="char" char="." rowspan="1" colspan="1">8.4</td><td align="char" char="." rowspan="1" colspan="1">40</td><td align="char" char="." rowspan="1" colspan="1">7</td><td align="char" char="." rowspan="1" colspan="1">23</td><td rowspan="1" colspan="1">NC_004823</td></tr><tr><td rowspan="1" colspan="1"> <italic>Theileria parva</italic></td><td align="char" char="." rowspan="1" colspan="1">39.6</td><td align="char" char="." rowspan="1" colspan="1">38.3</td><td align="char" char="." rowspan="1" colspan="1">43</td><td align="char" char="." rowspan="1" colspan="1">0</td><td align="char" char="." rowspan="1" colspan="1">21</td><td rowspan="1" colspan="1">NC_007758</td></tr><tr><td rowspan="1" colspan="1"> <italic>Toxoplasma gondii</italic></td><td align="char" char="." rowspan="1" colspan="1">35</td><td align="char" char="." rowspan="1" colspan="1">19.3</td><td align="char" char="." rowspan="1" colspan="1">44</td><td align="char" char="." rowspan="1" colspan="1">0</td><td align="char" char="." rowspan="1" colspan="1">21</td><td rowspan="1" colspan="1">NC_001799</td></tr><tr><td rowspan="1" colspan="1"> <italic>Chromera velia</italic></td><td align="char" char="." rowspan="1" colspan="1">119.8</td><td align="char" char="." rowspan="1" colspan="1">31.4</td><td align="char" char="." rowspan="1" colspan="1">84</td><td align="char" char="." rowspan="1" colspan="1">5</td><td align="char" char="." rowspan="1" colspan="1">25</td><td rowspan="1" colspan="1">NC_014340</td></tr><tr><td rowspan="1" colspan="1"> <italic>Alveolata</italic> sp. CCMP3155</td><td align="char" char="." rowspan="1" colspan="1">85.5</td><td align="char" char="." rowspan="1" colspan="1">13.6</td><td align="char" char="." rowspan="1" colspan="1">99</td><td align="char" char="." rowspan="1" colspan="1">2</td><td align="char" char="." rowspan="1" colspan="1">25</td><td rowspan="1" colspan="1">NC_014345</td></tr><tr><td rowspan="1" colspan="1"> <italic>Porphyra purpurea</italic></td><td align="char" char="." rowspan="1" colspan="1">191</td><td align="char" char="." rowspan="1" colspan="1">24.2</td><td align="char" char="." rowspan="1" colspan="1">218</td><td align="char" char="." rowspan="1" colspan="1">0</td><td align="char" char="." rowspan="1" colspan="1">35</td><td rowspan="1" colspan="1">NC_000925</td></tr><tr><td colspan="7" rowspan="1">Peridin-containing dinoflagellates<xref ref-type="table-fn" rid="tblfn4">d</xref></td></tr><tr><td rowspan="1" colspan="1"> <italic>Amphidinium operculatum</italic></td><td align="char" char="." rowspan="1" colspan="1">34.2</td><td align="char" char="." rowspan="1" colspan="1">64.2</td><td align="char" char="." rowspan="1" colspan="1">18</td><td align="char" char="." rowspan="1" colspan="1">0</td><td align="char" char="." rowspan="1" colspan="1">1</td><td rowspan="1" colspan="1"><xref ref-type="bibr" rid="bib5">Barbrook, Santucci, et al. (2006)</xref></td></tr></tbody></table><table-wrap-foot><fn><p>N<sc>OTE</sc>.—<italic>P. aphrodite</italic>, <italic>N. tabacum</italic>, <italic>E. gracilis</italic>, <italic>C. velia</italic>, <italic>Alveolata</italic> sp., <italic>P. purpurea</italic>, and <italic>A. operculatum</italic> are photosynthetic organisms while others are parasitic or heterotrophic.</p></fn><fn id="tblfn1"><label>a</label><p>Including structural RNAs but not introns. Only ORFs conserved in at least two plastid genomes were included.</p></fn><fn id="tblfn2"><label>b</label><p>Number of genes including structural RNAs and ORFs conserved in at least two plastid genomes. Duplicated genes were counted as one.</p></fn><fn id="tblfn3"><label>c</label><p>Duplicated tRNAs were counted as one.</p></fn><fn id="tblfn4"><label>d</label><p>The plastome of these organisms is fragmented into several plasmids.</p></fn></table-wrap-foot></table-wrap><fig id="fig2" position="float"><label>F<sc>IG</sc>. 2.</label><caption><p><italic>Rhizanthella gardneri</italic> plastid genome. Exons are displayed as blue arrows, introns as lines joining exons, tRNAs as black triangles, rRNAs in red, IRs as yellow arrows, and fragments or pseudogenes in orange. Ψ: pseudogenes. frag: fragment.</p></caption><graphic xlink:href="molbiolevolmsr028f02_4c"></graphic></fig><p>The <italic>R. gardneri</italic> plastome contains only 37 genes (including duplicates within the repeats) encoding 20 proteins, 4 rRNAs, and 9 transfer RNAs (<xref ref-type="table" rid="tbl2">table 2</xref>). In comparison, the <italic>P. aphrodite</italic> plastome contains 110 genes (<xref ref-type="bibr" rid="bib14">Chang et al. 2006</xref>), the plastome of <italic>E. virginiana</italic> contains 53 (<xref ref-type="bibr" rid="bib66">Wolfe et al. 1992</xref>) and even the highly reduced genomes of <italic>Toxoplasma gondii</italic> (35 kb; NC 001799) or the parasitic green alga <italic>Helicosporidium</italic> sp. (37.5 kb; <xref ref-type="bibr" rid="bib18">de Koning and Keeling 2006</xref>) contain 65 and 54, respectively. With the exception of the very peculiar plastid genomes of the peridin-containing dinoflagellates that are fragmented into several plasmids (<xref ref-type="bibr" rid="bib6">Barbrook, Santucci, et al. 2006</xref>; <xref ref-type="bibr" rid="bib28">Howe et al. 2008</xref>), the <italic>R. gardneri</italic> plastid is the most gene-poor plastid genome characterized so far (<xref ref-type="table" rid="tbl1">table 1</xref>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 2</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online). It contains fewer genes than any other characterized genetic system in land plants. In comparison with the plastome of <italic>P. aphrodite</italic>, which can be taken to resemble that of the photosynthetic ancestor of <italic>R. gardneri</italic>, an estimated 70% of the original genes were lost or transferred to the nucleus after the switch to a parasitic nonphotosynthetic lifestyle. These missing genes include those coding for the plastid-encoded RNA polymerase (PEP), the maturase-like protein MatK, all the genes required for photosynthesis (encoding subunits of photosystem I, photosystem II, cytochrome <italic>b</italic><sub>6</sub><italic>f</italic> complex, and ATP synthase), as well as 6 genes encoding ribosomal proteins and 27 genes encoding tRNAs. Some of these missing genes may have been transferred to the nucleus. Although no unambiguous examples of this could be found in the sequencing data set, we cannot rule out the eventuality because of the low coverage of the nuclear genome.</p><table-wrap id="tbl2" position="float"><label>Table 2.</label><caption><p>Gene Contents of Selected Plastomes.</p></caption><table frame="hsides" rules="groups"><thead><tr><td rowspan="1" colspan="1"></td><td colspan="4" align="center" rowspan="1">Photosynthesis<hr></hr></td><td rowspan="1" colspan="1"></td><td colspan="4" align="center" rowspan="1">Protein Synthesis<hr></hr></td><td rowspan="1" colspan="1"></td><td colspan="4" align="center" rowspan="1">Transfer RNA Genes<hr></hr></td></tr><tr><td rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"><italic>Pa</italic></td><td align="center" rowspan="1" colspan="1"><italic>Rg</italic></td><td align="center" rowspan="1" colspan="1"><italic>Cg</italic></td><td align="center" rowspan="1" colspan="1"><italic>Ev</italic></td><td rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"><italic>Pa</italic></td><td align="center" rowspan="1" colspan="1"><italic>Rg</italic></td><td align="center" rowspan="1" colspan="1"><italic>Cg</italic></td><td align="center" rowspan="1" colspan="1"><italic>Ev</italic></td><td rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1"><italic>Pa</italic></td><td align="center" rowspan="1" colspan="1"><italic>Rg</italic></td><td align="center" rowspan="1" colspan="1"><italic>Cg</italic></td><td align="center" rowspan="1" colspan="1"><italic>Ev</italic></td></tr></thead><tbody><tr><td rowspan="1" colspan="1"><italic>atpA</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1"><italic>infA</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1"><italic>trnA-ugc</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1">Ψ</td></tr><tr><td rowspan="1" colspan="1"><italic>atpB</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1"><bold><italic>rpl2</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><italic>trnC-gca</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">Ψ</td></tr><tr><td rowspan="1" colspan="1"><italic>atpE</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>rpl14</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1"><bold><italic>trnD-guc</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td></tr><tr><td rowspan="1" colspan="1"><italic>atpF</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>rpl16</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold><italic>trnE-uuc</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td></tr><tr><td rowspan="1" colspan="1"><italic>atpH</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>rpl20</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold><italic>trnF-gaa</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td></tr><tr><td rowspan="1" colspan="1"><italic>atpI</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>rpl22</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>trnfM-cau</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td></tr><tr><td rowspan="1" colspan="1"><italic>ccsA</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>rpl23</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1"><italic>trnG-gcc</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td></tr><tr><td rowspan="1" colspan="1"><italic>cemA</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>rpl32</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>trnG-ucc</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1">−</td></tr><tr><td rowspan="1" colspan="1"><italic>petA</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>rpl33</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1"><italic>trnH-gug</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td></tr><tr><td rowspan="1" colspan="1"><italic>petB</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>rpl36</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold><italic>trnI-cau</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td></tr><tr><td rowspan="1" colspan="1"><italic>petD</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>rps2</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><italic>trnI-gau</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1">Ψ</td></tr><tr><td rowspan="1" colspan="1"><italic>petG</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>rps3</italic></bold></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1"><italic>trnK-uuu</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td></tr><tr><td rowspan="1" colspan="1"><italic>petL</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>rps4</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><italic>trnL-caa</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td></tr><tr><td rowspan="1" colspan="1"><italic>petN</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>rps7</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><italic>trnL-uaa</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td></tr><tr><td rowspan="1" colspan="1"><italic>psaA</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>rps8</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><italic>trnL-uag</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td></tr><tr><td rowspan="1" colspan="1"><italic>psaB</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>rps11</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><italic>trnM-cau</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td></tr><tr><td rowspan="1" colspan="1"><italic>psaC</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>rps12</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1"><italic>trnN-guu</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td></tr><tr><td rowspan="1" colspan="1"><italic>psaI</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>rps14</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1"><italic>trnP-ugg</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td></tr><tr><td rowspan="1" colspan="1"><italic>psaJ</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>rps15</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>trnQ-uug</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td></tr><tr><td rowspan="1" colspan="1"><italic>psbA</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1"><italic>rps16</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>trnR-acg</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1">+</td></tr><tr><td rowspan="1" colspan="1"><italic>psbB</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1"><bold><italic>rps18</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><italic>trnR-ucu</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">Ψ</td></tr><tr><td rowspan="1" colspan="1"><italic>psbC</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>rps19</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><italic>trnS-gcu</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td></tr><tr><td rowspan="1" colspan="1"><italic>psbD</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"></td><td colspan="4" rowspan="1"><bold>RNA Metabolism</bold></td><td rowspan="1" colspan="1"><italic>trnS-gga</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">Ψ</td></tr><tr><td rowspan="1" colspan="1"><italic>psbE</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"><italic>Pa</italic></td><td rowspan="1" colspan="1"><italic>Rg</italic></td><td rowspan="1" colspan="1"><italic>Cg</italic></td><td rowspan="1" colspan="1"><italic>Ev</italic></td><td rowspan="1" colspan="1"><italic>trnS-uga</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">+</td></tr><tr><td rowspan="1" colspan="1"><italic>psbF</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>matK</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1"><italic>trnT-ggu</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td></tr><tr><td rowspan="1" colspan="1"><italic>psbH</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>rpoA</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1"><italic>trnT-ugu</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td></tr><tr><td rowspan="1" colspan="1"><italic>psbI</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>rpoB</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>trnV-gac</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td></tr><tr><td rowspan="1" colspan="1"><italic>psbJ</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>rpoC1</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>trnV-uac</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td></tr><tr><td rowspan="1" colspan="1"><italic>psbK</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><italic>rpoC2</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>trnW-cca</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td></tr><tr><td rowspan="1" colspan="1"><italic>psbL</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"></td><td colspan="4" rowspan="1"><bold>Essential Genes</bold></td><td rowspan="1" colspan="1"><bold><italic>trnY-gua</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1">+</td></tr><tr><td rowspan="1" colspan="1"><italic>psbM</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"><italic>Pa</italic></td><td rowspan="1" colspan="1"><italic>Rg</italic></td><td rowspan="1" colspan="1"><italic>Cg</italic></td><td rowspan="1" colspan="1"><italic>Ev</italic></td><td rowspan="1" colspan="1"></td><td colspan="4" rowspan="1"><bold>Ribosomal RNA Genes</bold></td></tr><tr><td rowspan="1" colspan="1"><italic>psbN</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>clpP</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"><italic>Pa</italic></td><td rowspan="1" colspan="1"><italic>Rg</italic></td><td rowspan="1" colspan="1"><italic>Cg</italic></td><td rowspan="1" colspan="1"><italic>Ev</italic></td></tr><tr><td rowspan="1" colspan="1"><italic>psbT</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>accD</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold><italic>rrn16</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td></tr><tr><td rowspan="1" colspan="1"><italic>rbcL</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">Ψ</td><td rowspan="1" colspan="1"><bold><italic>ycf1</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold><italic>rrn23</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td></tr><tr><td rowspan="1" colspan="1"><italic>psbZ</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"><bold><italic>ycf2</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold><italic>rrn4.5</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td></tr><tr><td rowspan="1" colspan="1"><italic>ycf3</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"><bold><italic>rrn5</italic></bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td><td rowspan="1" colspan="1"><bold>+</bold></td></tr><tr><td rowspan="1" colspan="1"><italic>ycf4</italic></td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1">+</td><td rowspan="1" colspan="1">−</td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td></tr></tbody></table><table-wrap-foot><fn><p>N<sc>OTE.</sc>—<italic>Pa</italic>, <italic>Phalaenopsis aphrodite</italic>; <italic>Rg</italic>, <italic>Rhizanthella gardneri</italic>; <italic>Cg</italic>, <italic>Cuscuta gronovii</italic>; <italic>Ev</italic>, <italic>Epifagus virginiana</italic>; <italic>Ψ</italic>, pseudogene; +, present; −, missing. Genes present in all four plastomes are indicated in bold.</p></fn></table-wrap-foot></table-wrap><p>The loss of the <italic>rpo</italic> genes encoding the major RNA polymerase, PEP, is associated with sequence divergence in some of the remaining promoters. Among the <italic>R. gardneri</italic> plastid genes, some are transcribed both from nucleus-encoded polymerase (NEP) promoters and PEP promoters in <italic>Arabidopsis thaliana</italic> (<xref ref-type="bibr" rid="bib58">Swiatecka-Hagenbruch et al. 2007</xref>). The analysis of the corresponding upstream sequences in <italic>R. gardneri</italic> (<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary fig. 2</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online) showed that the putative PEP promoters are not conserved in the sequences upstream of the <italic>rps4</italic> and <italic>rrn16</italic> genes but are apparently still present upstream of <italic>ycf1</italic>. NEP promoter motifs are conserved in the promoters of <italic>ycf1</italic>, <italic>rps4</italic>, and <italic>clpP</italic> but have diverged upstream of <italic>rrn16</italic>.</p><p>Sixteen of the <italic>R. gardneri</italic> genes encode proteins of the translation machinery (6 <italic>rpl</italic> genes, 9 <italic>rps</italic> genes, and an initiation factor); the other four protein-encoding genes are <italic>accD</italic>, <italic>ycf1</italic>, <italic>ycf2</italic>, and <italic>clpP</italic>, all easily identified by homology to plastid genes from other plants. Despite the reduced tRNA set, there is no significant change in codon usage compared with <italic>P. aphrodite</italic> (<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 3</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online).</p><p>The clustering of 172 complete plastid genomes based on their gene content (<xref ref-type="fig" rid="fig3">fig. 3</xref>) shows that plastomes deriving from green or red algae form two distinct groups, apart from some heterotrophs. These latter species derive either from green algae (<italic>Euglena longa</italic>, <italic>Helicosporidium</italic> sp., <italic>E. virginiana</italic>, and <italic>R. gardneri</italic>) or red algae (<italic>Eimeria tenella</italic>, <italic>T. gondii</italic>, and <italic>Theileria parva</italic>; <xref ref-type="bibr" rid="bib29">Janouskovec et al. 2010</xref>) but cluster together. Some parasitic plants or algae (<italic>Cuscuta</italic> species, <italic>Aneura mirabilis</italic> and <italic>Cryptomonas paramecium</italic>) are not part of this cluster. However, these have either not completely switched to a nonphotosynthetic lifestyle (<xref ref-type="bibr" rid="bib27">Hibberd et al. 1998</xref>) or did so only recently (<xref ref-type="bibr" rid="bib63">Wickett et al. 2008</xref>; <xref ref-type="bibr" rid="bib21">Donaher et al. 2009</xref>).</p><fig id="fig3" position="float"><label>F<sc>IG</sc>. 3.</label><caption><p>Convergence of plastid genomes from parasites. One-hundred and seventy-two plastid genomes were clustered by Bayesian inference using the data in <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 1</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online. Black triangles indicate collapsed clusters, with the number and taxonomic group of the species shown. Probabilities above 0.6 are shown at the corresponding nodes. Red, green, and blue branches indicate plastids derived from the red, green, and blue lineage, respectively. <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary data 1</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online, is the full tree in NEXUS format.</p></caption><graphic xlink:href="molbiolevolmsr028f03_4c"></graphic></fig><p>Comparison of DNA sequences from the central and southern populations of <italic>R. gardneri</italic> showed that the plastome is accumulating mutations at a very high rate, at least 15-fold faster than the mitochondrial genome (<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 4</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online). This result is in line with the increased rates of fixation of plastid DNA mutations described in other parasitic plants (<xref ref-type="bibr" rid="bib69">Young and dePamphilis 2005</xref>). The sequence divergence observed between the two populations of <italic>R. gardneri</italic> are similar to those observed between different species of <italic>Cuscuta</italic> (<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 5</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online). The relative rate of divergence of the <italic>R. gardneri rrn23</italic> gene is higher than that of the <italic>rps8</italic> and <italic>rpl36</italic> genes when compared with the equivalent rates in the <italic>Cuscuta</italic> species (<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 5</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online).</p><p>Despite this high rate of sequence divergence in the <italic>R. gardneri</italic> plastome, preferential conservation of the coding sequences (<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 4</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online) suggests that the genes are expressed and functional. We cloned <italic>rpl2</italic>, <italic>rpl16</italic>, and <italic>clpP</italic> cDNAs (accession numbers GU066223, GU066224, and GU066222, respectively). These three cDNAs were correctly spliced showing that RNA splicing is occurring in <italic>R. gardneri</italic> plastids. Within these mRNAs, we detected two C–U editing events: at the start codon of <italic>rpl2</italic> and in the second exon of <italic>rpl16</italic> (<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary fig. 3</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online). Hence, <italic>R. gardneri</italic> has normal plastid RNA metabolism with transcription, splicing, and editing occurring.</p></sec><sec sec-type="discussion"><title>Discussion</title><p>The <italic>R. gardneri</italic> plastid contains a typical quadripartite genome with reduced IRs. This reduction has resulted in the presence of a single copy of the <italic>rrn</italic> genes as opposed to duplicates or even triplicates in all other plastomes containing large repeats (<xref ref-type="bibr" rid="bib57">Strauss et al. 1988</xref>; <xref ref-type="bibr" rid="bib13">Cai et al. 2008</xref>). Genes in the IRs generally display lower substitution rates compared with genes present in the single-copy regions (<xref ref-type="bibr" rid="bib65">Wolfe et al. 1987</xref>; <xref ref-type="bibr" rid="bib48">Perry and Wolfe 2002</xref>; <xref ref-type="bibr" rid="bib50">Raubeson et al. 2007</xref>). The relative divergence rates within the <italic>R. gardneri</italic> plastid genome (compared with parasitic <italic>Cuscuta</italic> species) is higher for the <italic>rrn23</italic> gene (duplicated in <italic>Cuscuta</italic>) than for the <italic>rps8</italic> and <italic>rpl36</italic> genes (single copy in all plastid genomes). This acceleration of mutation rates in the <italic>rrn</italic> genes in <italic>R. gardneri</italic> probably results from the loss of the duplicate copies as shown in legumes (<xref ref-type="bibr" rid="bib48">Perry and Wolfe 2002</xref>).</p><p>The reduction of the IRs is the major reason that explains why the <italic>R. gardneri</italic> plastome is smaller than that of the smallest previously known land plant plastid genome and that of the parasitic dicot <italic>E. virginiana.</italic> Despite the very small gene set encoded in this genome, it is not the smallest in size. Plastid genomes from apicomplexan parasites such as <italic>E. tenella</italic> or the parasitic green alga <italic>Helicosporidium</italic> sp. are much smaller in size, although they contain more genes (<xref ref-type="table" rid="tbl1">table 1</xref>).</p><p>The <italic>R. gardneri</italic> plastome contains one of the smallest gene sets characterized in any plastome analyzed so far. Only peridin-containing dinoflagellates possess plastids with less genes (<xref ref-type="bibr" rid="bib6">Barbrook, Santucci, et al. 2006</xref>; <xref ref-type="bibr" rid="bib28">Howe et al. 2008</xref>). Despite rampant gene loss, the <italic>R. gardneri</italic> plastome appears to be the basis of a functioning gene expression system, with transcription, splicing, and RNA editing all detected and translation likely. Although editing requires only nuclear-encoded factors (<xref ref-type="bibr" rid="bib53">Schmitz-Linneweber and Small 2008</xref>), transcription in land plant plastids usually relies on two distinct transcription machineries: One encoded by the nucleus (NEP) and the other encoded in part by the plastid. The <italic>rpo</italic> genes coding for the PEP are missing in <italic>R. gardneri</italic>. In photosynthetic plastids, each polymerase transcribes a distinct but overlapping set of genes (<xref ref-type="bibr" rid="bib26">Hajdukiewicz et al. 1997</xref>), with PEP preferentially transcribing photosynthesis-related genes. As no gene typically relying exclusively on PEP for its transcription remains in the <italic>Rhizanthella</italic> plastid genome, the loss of <italic>rpo</italic> genes in <italic>R. gardneri</italic> can be understood. The loss of PEP probably explains the divergence noted in the promoter regions of several of the remaining genes (<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary fig. 2</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online).</p><p>Splicing of introns in chloroplasts requires several nuclearly encoded factors that are specific to one or more introns (<xref ref-type="bibr" rid="bib4">Asakura and Barkan 2006</xref>; <xref ref-type="bibr" rid="bib19">de Longevialle et al. 2008</xref>). The chloroplast genome also encodes a maturase-like protein, MatK, which is involved in splicing of the <italic>trnK</italic> intron in which it is embedded (<xref ref-type="bibr" rid="bib61">Vogel et al. 1997</xref>) but is probably also required for the splicing of the group IIa subset of plastid introns (<xref ref-type="bibr" rid="bib30">Jenkins et al. 1997</xref>; <xref ref-type="bibr" rid="bib60">Vogel et al. 1999</xref>; <xref ref-type="bibr" rid="bib23">Duffy et al. 2009</xref>; <xref ref-type="bibr" rid="bib46">McNeal et al. 2009</xref>). The loss of <italic>matK</italic> has been observed in <italic>Cuscuta</italic> species from the subgenus <italic>Grammica</italic>, which have also lost the introns thought to require MatK activity. The loss of <italic>matK</italic> in <italic>R. gardneri</italic> is more surprising because the <italic>R. gardneri</italic> plastid genome has retained three group IIa introns, two of which we show to be correctly spliced and which, in tobacco, are bound by MatK (<xref ref-type="bibr" rid="bib71">Zoschke et al. 2010</xref>). A large proportion of <italic>matK</italic> genes in orchids are pseudogenes because of unequal insertions/deletions (<xref ref-type="bibr" rid="bib38">Kores et al. 2000</xref>, <xref ref-type="bibr" rid="bib37">2001</xref>) suggesting that the role of <italic>matK</italic> for splicing in this family of plants is not as essential as in other families. This may explain why <italic>matK</italic> has been lost in <italic>R. gardneri</italic> without impairing splicing of the remaining group IIa introns.</p><p>Plastid translation is generally required for cell viability from embryogenesis onward in land plants (<xref ref-type="bibr" rid="bib8">Berg et al. 2005</xref>), and we presume that this is the case in <italic>R. gardneri</italic>, despite the loss of many genes normally essential for translation to occur. The missing proteins are most probably imported along with other elements of the translation machinery already imported into plastids in other plants (<xref ref-type="bibr" rid="bib55">Stengel et al. 2007</xref>). Most striking of all, the <italic>R. gardneri</italic> plastome is characterized by the loss of a large proportion of tRNA genes: Only 10 genes coding for 9 different tRNAs are present (<xref ref-type="table" rid="tbl2">table 2</xref>). This is by far the smallest tRNA set in an unfragmented plastid genome (<xref ref-type="table" rid="tbl1">table 1</xref>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 2</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online) and manifestly insufficient for translation. Despite this reduced tRNA set, there is no significant change in codon usage compared with <italic>P. aphrodite</italic> (<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 3</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online).</p><p>Import of cytosolic tRNAs into plastids has never been directly demonstrated and several lines of evidence suggest that it does not occur in photosynthetic land plants (<xref ref-type="bibr" rid="bib44">Lung et al. 2006</xref>; <xref ref-type="bibr" rid="bib51">Rogalski et al. 2008</xref>), but we presume that the missing tRNAs are indeed imported, as also suggested for <italic>E. virginiana</italic> (<xref ref-type="bibr" rid="bib66">Wolfe et al. 1992</xref>). Cytosolic tRNAs are imported into mitochondria of land plants and there are intriguing parallels between the tRNA sets encoded in both organelles (<xref ref-type="bibr" rid="bib43">Lohan and Wolfe 1998</xref>): 25 of 30 tRNAs are either sometimes imported into mitochondria and not conserved in parasite plastomes or never imported into mitochondria and conserved in plastomes (<xref ref-type="table" rid="tbl3">table 3</xref>). This implies that the same constraints apply for the import of tRNAs into both mitochondria and plastids. These constraints can be guessed at for all five tRNAs retained in all plant organelle genomes.</p><table-wrap id="tbl3" position="float"><label>Table 3.</label><caption><p>Plant Mitochondria and Plastids Tend to Lose and Retain the Same tRNA Genes.</p></caption><table frame="hsides" rules="groups"><thead><tr><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td colspan="3" align="center" rowspan="1">Mitochondria<hr></hr></td></tr><tr><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1">Always Conserved</td><td align="center" rowspan="1" colspan="1">Sometimes Replaced</td><td align="center" rowspan="1" colspan="1">Sometimes Lost</td></tr></thead><tbody><tr><td rowspan="2" colspan="1">Plastids</td><td rowspan="1" colspan="1">Always conserved</td><td rowspan="1" colspan="1">E-uuc; Q-uug; I-cau; fM-cau; Y-gua</td><td rowspan="1" colspan="1">D-guc</td><td rowspan="1" colspan="1">F-gaa; W-cca</td></tr><tr><td rowspan="1" colspan="1">Sometimes lost</td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1">eM-cau; N-guu; C-gca</td><td rowspan="1" colspan="1">S-gga; A-ugc; R-acg; G-gcc; R-ucu; G-ucc; T-ggu; I-gau; T-ugu; K-uuu; V-gac; L-uaa; V-uac; H-gug; L-uag; P-ugg; S-uga; S-gcu; L-caa</td></tr></tbody></table><table-wrap-foot><fn><p>N<sc>OTE</sc>.—Modified from (<xref ref-type="bibr" rid="bib43">Lohan and Wolfe 1998</xref>). tRNA genes are indicated by single letter amino acid codes and their anticodon sequence. “Sometimes replaced” indicates mitochondrial tRNA genes that have been replaced by orthologous plastid genes in horizontal gene transfer events.</p></fn></table-wrap-foot></table-wrap><p>Aminoacylated tRNA<sup>Glu</sup>(UUC) is a precursor not only for protein synthesis but also for tetrapyrrole synthesis (<xref ref-type="bibr" rid="bib59">Tanaka R and Tanaka A 2007</xref>). In photosynthetic plants, it is required for chlorophyll synthesis, and in all plants for the synthesis of heme for mitochondrial respiratory complexes and other essential proteins. Imported cytosolic tRNA<sup>Glu</sup> would therefore need to be recognized by not only glutamyl-tRNA synthetase for aminocylation but also glutamyl-tRNA reductase for tetrapyrrole synthesis. The <italic>trnE</italic> gene may be the primary justification for the presence of a genome in all nonphotosynthetic plastids (<xref ref-type="bibr" rid="bib5">Barbrook, Howe, et al. 2006</xref>). Similarly, tRNA<sup>fMet</sup> is required for initiating translation in prokaryotic systems, including virtually all organelles; imported tRNA<sup>Met</sup> would need to be recognized by the methionyl-tRNA transformylase or translation initiation factors in addition to being aminoacylated by methionine-tRNA synthetase. For both these tRNAs, the requirement for an imported replacement to be recognized by several distinct enzymes for which they are not normally substrates makes it extremely unlikely for functional replacement to occur.</p><p>The other three ubiquitous plant organellar tRNAs share unusual features about their aminoacylation that make them different from all other tRNAs. Organellar tRNA<sup>Ile</sup> (CAU) has a typical tRNA<sup>Met</sup> anticodon, but this is modified by addition of the amino acid lysidine to C<sub>34</sub>; the organellar isoleucyl-tRNA synthetase has evolved to recognize this unusual modified base which is not found in cytosolic tRNAs. Organellar tRNA<sup>Tyr</sup> differs extensively from its cytosolic counterpart in that it has a very long variable loop. For both these tRNAs, the imported equivalent would fail to be recognized by the corresponding organellar aminoacyl-tRNA synthetase. Plant organellar tRNA<sup>Gln</sup>-Gln is formed by amidation of tRNA<sup>Gln</sup>-Glu; there is no glutaminyl-tRNA synthetase.</p><p>Thus for tRNA<sup>Ile</sup>(CAU), tRNA<sup>Tyr</sup>, and tRNA<sup>Gln</sup>, import of the cytosolic tRNA alone would be unlikely to lead to functional aminoacyl-tRNA for translation. Only coupled import of a suitable aminoacyl-tRNA synthetase could establish functional replacement of the organellar genes. Incidentally, the convergences noted here between retention of plastid and mitochondrial tRNA genes argues that unlike some early suggestions, coupled transport of tRNAs and aminoacyl-tRNA synthetases is probably not the mechanism by which organellar tRNA import occurs.</p><p>Apart from genes involved in the translation machinery (rRNAs, ribosomal proteins, and tRNAs), <italic>R. gardneri</italic> has retained a very restricted set of other protein-coding genes, namely <italic>ycf1</italic>, <italic>ycf2</italic>, <italic>accD</italic>, and <italic>clpP</italic> (<xref ref-type="table" rid="tbl2">table 2</xref>). <italic>accD</italic>, <italic>ycf1</italic>, and <italic>ycf2</italic> are conserved in almost all land plants (<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 2</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online) but have been lost in grasses (<xref ref-type="bibr" rid="bib31">Katayama and Ogihara 1996</xref>) and <italic>accD</italic> is missing in a few other lineages (<xref ref-type="bibr" rid="bib33">Knox and Palmer 1999</xref>; <xref ref-type="bibr" rid="bib15">Chumley et al. 2006</xref>). The <italic>accD</italic> gene encodes the carboxyltransferase subunit of a multimeric acetyl-CoA carboxylase (ACCase), which provides malonyl-CoA for the biosynthesis of fatty acids. These fatty acids are then used for the synthesis of every cellular membrane (<xref ref-type="bibr" rid="bib7">Benning et al. 2006</xref>). This fundamental function may explain why mutations in <italic>accD</italic> (<xref ref-type="bibr" rid="bib34">Kode et al. 2005</xref>) or in the plastid translation machinery (<xref ref-type="bibr" rid="bib8">Berg et al. 2005</xref>; <xref ref-type="bibr" rid="bib51">Rogalski et al. 2008</xref>) are lethal. In the few plants where this is not the case, an imported monomeric ACCase replaces the requirement for the <italic>accD</italic> gene product (<xref ref-type="bibr" rid="bib36">Konishi et al. 1996</xref>). The essential functions of <italic>ycf1</italic> and <italic>ycf2</italic> are unknown (<xref ref-type="bibr" rid="bib22">Drescher et al. 2000</xref>) but might possibly be linked to expression, assembly, or function of the <italic>accD</italic> gene product, given that grasses have lost both genes in addition to <italic>accD</italic>. Other plants that have lost <italic>accD</italic> have divergent <italic>ycf1</italic> and <italic>ycf2</italic> sequences.</p><p>Finally, <italic>clpP</italic> is the only protein-coding gene present in all land plant and green algal plastomes except for that of the parasitic alga <italic>Helicosporidium</italic> sp. (<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 2</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online). It codes for a catalytic subunit of a multimeric protease. In land plants, <italic>clpP</italic> is essential (<xref ref-type="bibr" rid="bib39">Kuroda and Maliga 2003</xref>) but which of its varied roles are required remains unclear. Recent studies suggest that a function in the regulation of an array of processes including isoprenoid and tetrapyrrole biosynthesis, lipid body stability, and photosynthesis (<xref ref-type="bibr" rid="bib32">Kim et al. 2009</xref>; <xref ref-type="bibr" rid="bib54">Stanne et al. 2009</xref>; <xref ref-type="bibr" rid="bib72">Zybailov et al. 2009</xref>).</p><p>The <italic>R. gardneri</italic> plastome is also informative on the selective pressures acting to retain certain genes within organelle genomes. The small number of retained genes and relative lack of pseudogenes (5 vs. 18 in <italic>E. virginiana</italic>) suggests that the <italic>R. gardneri</italic> plastome has progressed further toward shedding or transferring nonessential genes than any other land plant organelle examined so far. The loss of photosynthetic capacity is associated with a strong reduction of the plastid coding capacity, in line with the evolutionary trend of genome reduction in plastids (<xref ref-type="bibr" rid="bib45">Martin et al. 1998</xref>). The remaining gene set is clearly not random. The analysis of the plastid gene content in 172 organisms (<xref ref-type="fig" rid="fig3">fig. 3</xref>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary table 2</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary Material</ext-link> online) showed the remarkable similarity of the apicomplexans and parasitic plants. We believe this similarity primarily reflects convergent rather than shared evolution given the supposed evolutionary distance between these plastid genomes. We note, however, that although several lines of evidence strongly support a red algal origin for apicoplasts (<xref ref-type="bibr" rid="bib64">Wilson et al. 1996</xref>; <xref ref-type="bibr" rid="bib68">Yoon et al. 2002</xref>; <xref ref-type="bibr" rid="bib29">Janouskovec et al. 2010</xref>), it is still a matter of controversy (<xref ref-type="bibr" rid="bib35">Kohler et al. 1997</xref>; <xref ref-type="bibr" rid="bib42">Lau et al. 2009</xref>). It has been noted previously (<xref ref-type="bibr" rid="bib56">Stiller et al. 2003</xref>) that, when considering ribosomal proteins and tRNAs, similarities in plastid gene content reflect convergent evolution rather than shared descent. The similarity of the plastid gene contents of nonphotosynthetic organisms suggests that they tend to converge toward a distinct shared gene set given enough time. The nature of this set gives clues about the evolutionary constraints on plastid gene losses.</p><p>What are these constraints? The most popular previously suggested explanations (<xref ref-type="bibr" rid="bib16">Daley and Whelan 2005</xref>; <xref ref-type="bibr" rid="bib5">Barbrook, Howe, et al. 2006</xref>) revolve around constraints on protein import due to high hydrophobicity (<xref ref-type="bibr" rid="bib17">de Grey 2005</xref>) or essential regulation of gene expression by reactive oxygen signaling cascades (<xref ref-type="bibr" rid="bib2">Allen et al. 2005</xref>; <xref ref-type="bibr" rid="bib28">Howe et al. 2008</xref>). However, they cannot easily account for the retention of <italic>accD</italic> and <italic>clpP</italic>, which encode typical soluble globular proteins that are not involved in respiration or photosynthesis. An alternative hypothesis suggests that certain genes encoding key products required for controlling the assembly of multiprotein complexes cannot be easily lost or transferred (<xref ref-type="bibr" rid="bib70">Zerges 2002</xref>). This could be explained by “control by epistasy of synthesis” (<xref ref-type="bibr" rid="bib67">Wostrikoff et al. 2004</xref>) which is an elegant theory on the regulation of assembly of protein complexes that requires at least one subunit to be organelle encoded. The <italic>accD</italic> and <italic>clpP</italic> gene products are both essential components of large protein complexes that must be assembled within the plastid. We postulate that herein lies the explanation for the very small retained gene set of the <italic>R. gardneri</italic> plastome.</p></sec><sec sec-type="supplementary-material"><title>Supplementary Material</title><p><ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">Supplementary tables 1</ext-link>–<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">5</ext-link>, <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">figures 1</ext-link>–<ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">3</ext-link>, and <ext-link ext-link-type="uri" xlink:href="http://mbe.oxfordjournals.org/cgi/content/full/msr028/DC1">supplementary data 1</ext-link> are available at <italic>Molecular Biology and Evolution</italic> online (<ext-link ext-link-type="uri" xlink:href="http://www.mbe.oxfordjournals.org/">http://www.mbe.oxfordjournals.org/</ext-link>).</p>
<supplementary-material id="PMC_1" content-type="local-data"><caption><title>Supplementary Data</title></caption><media mimetype="text" mime-subtype="html" xlink:href="supp_28_7_2077__index.html"></media><media xlink:role="associated-file" mimetype="application" mime-subtype="pdf" xlink:href="supp_msr028_supp_fig1.pdf"></media><media xlink:role="associated-file" mimetype="application" mime-subtype="pdf" xlink:href="supp_msr028_supp_fig2.pdf"></media><media xlink:role="associated-file" mimetype="application" mime-subtype="pdf" xlink:href="supp_msr028_supp_fig3-editing.pdf"></media><media xlink:role="associated-file" mimetype="text" mime-subtype="plain" xlink:href="supp_msr028_suppdata1.txt"></media><media xlink:role="associated-file" mimetype="application" mime-subtype="vnd.ms-excel" xlink:href="supp_msr028_supptable2.xls"></media><media xlink:role="associated-file" mimetype="application" mime-subtype="msword" xlink:href="supp_msr028_supp_tables1-3-4.doc"></media></supplementary-material></sec></body><back><ack><p>This work was supported by the <funding-source>Australian Research Council Centre of Excellence</funding-source> in Plant Energy Biology (grant <award-id>CE0561495</award-id>) and a grant from the <funding-source>Faculty of Natural Science and Agriculture of the University of Western Australia</funding-source>. M.B. is supported by Lotterywest funding for the Wheatbelt Orchid Rescue Project. I.S. was supported by the West Australian Premier's Fellowship scheme. 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